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GENOMICS, MOLECULAR GENETICS & BIOTECHNOLOGY

Microsatellite Markers Linked to Stem Rust Resistance Allele Sr9a in Wheat

^a Dep. of Agronomy and Plant Genetics, 411 Borlaug Hall, Univ. of Minnesota, St. Paul, MN 55108
^b USDA-ARS Cereal Disease Lab., 1551 Lindig Ave, Univ. of Minnesota, St. Paul, MN 55108

^* Corresponding author (ander319{at}umn.edu).

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Host resistance to stem rust of wheat (Triticum aestivum L.), caused by Puccinia graminis Pers.:Pers. f. sp. tritici Eriks. & E. Henn., is more effective and durable when several stem rust resistance (Sr) genes are pyramided into a single line. We studied the Sr9a allele, one of six known alleles at the Sr9 locus on chromosome 2BL, using 116 F₂ plants and their F_2:3 families derived from the cross of near-isogenic lines (NILs) ‘Chinese Spring’ and ISr9a-Ra. Four microsatellite markers were identified that mapped within 3.6 cM proximal to the Sr9a locus. Fifty-nine wheat accessions were screened with the three codominant and one dominant markers to determine their polymorphism information content (PIC). The marker Xgwm47 revealed 12 alleles and had the highest PIC value of 0.85. We attempted to postulate the presence of Sr9a by phenotypic screening. In accessions that had multiple Sr genes, however, it was not possible to postulate Sr9a due to masking effects. Despite the ambiguity of phenotypic evaluation, Xgwm47 was diagnostic for Sr9a in additional NILs tested. These results suggest that Xgwm47 will be a useful tool for marker-assisted selection of Sr9a in wheat breeding programs.

Abbreviations: bp, base pairs • cM, centimorgan • MAS, marker-assisted selection • NIL, near-isogenic lines • PIC, polymorphism information content • SSR, simple sequence repeat

Microsatellite Markers Linked to Stem Rust Resistance Allele Sr9a in Wheat

^a Dep. of Agronomy and Plant Genetics, 411 Borlaug Hall, Univ. of Minnesota, St. Paul, MN 55108
^b USDA-ARS Cereal Disease Lab., 1551 Lindig Ave, Univ. of Minnesota, St. Paul, MN 55108

^* Corresponding author (ander319{at}umn.edu).

Host resistance to stem rust of wheat (Triticum aestivum L.), caused by Puccinia graminis Pers.:Pers. f. sp. tritici Eriks. & E. Henn., is more effective and durable when several stem rust resistance (Sr) genes are pyramided into a single line. We studied the Sr9a allele, one of six known alleles at the Sr9 locus on chromosome 2BL, using 116 F₂ plants and their F_2:3 families derived from the cross of near-isogenic lines (NILs) ‘Chinese Spring’ and ISr9a-Ra. Four microsatellite markers were identified that mapped within 3.6 cM proximal to the Sr9a locus. Fifty-nine wheat accessions were screened with the three codominant and one dominant markers to determine their polymorphism information content (PIC). The marker Xgwm47 revealed 12 alleles and had the highest PIC value of 0.85. We attempted to postulate the presence of Sr9a by phenotypic screening. In accessions that had multiple Sr genes, however, it was not possible to postulate Sr9a due to masking effects. Despite the ambiguity of phenotypic evaluation, Xgwm47 was diagnostic for Sr9a in additional NILs tested. These results suggest that Xgwm47 will be a useful tool for marker-assisted selection of Sr9a in wheat breeding programs.

Abbreviations: bp, base pairs • cM, centimorgan • MAS, marker-assisted selection • NIL, near-isogenic lines • PIC, polymorphism information content • SSR, simple sequence repeat

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
STEM RUST of wheat (Triticum aestivum L.), caused by Puccinia graminis Pers.:Pers. f. sp. tritici Eriks. & E. Henn., is a very destructive disease of wheat, reaching devastating epidemic levels in most wheat-growing areas of the world (Knott, 1989). To date, more than 45 stem rust resistance (Sr) genes have been identified against different races of this fungus (McIntosh et al., 2003). Even though single-gene resistance may be overcome by the rapidly evolving races, the use of resistant cultivars is still the most effective and economical method of reducing yield losses due to stem rust (McIntosh, 1988). One way to increase the durability of stem rust resistance genes is to pyramid several Sr genes to increase broad-spectrum resistance to several races (Pederson and Leath, 1988). With conventional methods in wheat breeding programs, the continual pyramiding of genes in a single genotype will become difficult or even impossible when one or more genes in the background is effective against many races of the pathogen.

Plant breeders have been successful in using many race- specific stem rust resistance genes; however, they have not been able to fully exploit resistance conferred by the Sr9a allele in breeding programs (McIntosh et al., 1995). This has been due largely to problems of detecting it in the presence of other stem rust resistance genes. Moreover, the wheat cultivar Red Egyptian, the original source of Sr6, Sr8a, and Sr9a (Knott, 1957), has been widely used in many wheat breeding programs (Knott, 1989; McIntosh et al., 1995), and Sr6 has a masking effect on Sr9a. Another difficulty in diagnosing the presence of Sr9a is that its infection type is difficult to determine because it is dependent on the background of the cultivar and the particular race of the pathogen (Knott, 1989). Gene Sr9a confers moderate resistance against the race TPMK, one of the most predominant and devastating races of P. graminis f.sp. tritici in North America (McVey et al., 1996, 2002; Jin, 2005), and against other important races such as QCCJ and MCCF. Therefore, this allele is still valuable in North America. The allele was initially characterized as one of the six (identified with suffixes a–g with the exclusion of c) alleles at the Sr9 locus (Knott, 1989). Sears and Loegering (1968) mapped the Sr9 locus on the long arm of chromosome 2BL.

The potential benefits of molecular marker-assisted selection (MAS) have been widely discussed (Melchinger, 1990; Paterson et al., 1991; Young, 1996; Mohan et al., 1997; Anderson, 2003), especially to provide solutions to overcome some of the problems faced by classical phenotypic screening approaches in plant breeding programs. For example, to facilitate breeding for durable resistance to stem rust, molecular markers are useful tools in developing resistant cultivars and, especially, pyramiding several disease resistance genes (Anderson, 2003). Marker-assisted selection can be used at an early stage of plant development when multiple DNA markers are used to screen several genes simultaneously.

The objectives of this study were to: (i) determine the precise chromosomal location of the Sr9a allele based on genetic markers on 2BL; and (ii) identify codominant microsatellite markers closely linked to Sr9a that could be used for MAS.

	MATERIALS AND METHODS

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Plant Materials
Mapping of the Sr9a gene was performed by analysis of 116 F₂ individuals derived from a cross between the near-isogenic lines (NILs) ‘Chinese Spring’ as a female parent and ISr9a-Ra as a male parent. The ISr9a-Ra (CItr 14169) line is a BC₃F₁₁-derived line resulting from the cross of the original source of Sr9a, Red Egyptian, and Chinese Spring (CItr 14108) as the recurrent parent (Loegering and Harmon, 1969). The F₃ seed was obtained from self pollination (bagged spikes) of each F₂ plant. In addition to the mapping of Sr9a, a set of 59 wheat cultivars and breeding lines (Table 1 ) was analyzed to determine polymorphism information of markers and their usefulness as diagnostic markers for Sr9a. Seeds of wheat accessions were obtained from the USDA-ARS National Small Grains Collection, Aberdeen, ID. Seeds of breeding lines and germplasm were obtained from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN. This set of accessions included two additional pairs of NILs, Sr9a/9*LMPG (Knott, 1990) and ‘Marquis’9*/Red Egyptian (Knott, 1965), carrying the Sr9a allele in a different genetic background of LMPG and Marquis, respectively. Red Egyptian (CItr 12345), the original source of the Sr9a allele, was also included in the analysis. Because there were five different accessions of Red Egyptian in the NSGC database, all of them were included in the analysis. The Chinese Spring nullisomic–tetrasomic (N2B–T2D) line (Sears, 1966a) was used to determine the chromosomal location of the amplified bands of microsatellite markers.

DNA Extraction and Microsatellite Analysis
To investigate the linkage relationship between Sr9a and genetic markers, fresh leaf tissues were collected from young seedlings of the 116 F₂ individuals and 59 wheat accessions and breeding lines. Total genomic DNA was extracted following protocols described by Riede and Anderson (1996) and modified by Liu et al. (2006). Gene Sr9a was previously located on the long arm of chromosome 2B (Loegering and Harmon, 1969). Forty-four microsatellite primer pairs (GWM, WMC, CFD, and BARC) whose loci mapped on the long arm and centromere region of 2B (Röder et al., 1998; Somers et al., 2004; Song et al., 2005; see also www.scabusa.org/pdfs/BARC_SSRs_011101.html [verified 16 July 2007]) were used to screen for polymorphism between the parental lines that differed in their Sr9a allelic status. We used the primer pairs to screen for polymorphism between two pairs of NILs, ISr9a-Ra and Sr9a/9*LMPG, both carrying Sr9a in the genetic background of susceptible lines Chinese Spring and LMPG, respectively. To reveal linkage relationships between Sr9a and the microsatellite marker loci, all polymorphic simple sequence repeat (SSR) primer pairs were screened on the 116 F₂ plants.

Polymerase chain reaction (PCR) was performed in a 96-well plate with 10 µL of final reaction mixture containing 1 µL 10x PCR buffer, 25 mmol/L MgCl₂, 1.25 mmol/L dNTPs, 1 µmol/L of each primer, 5 units/µL Taq DNA polymerase (Applied Biosystems, Branchburg, NJ), and 15 mg/L genomic DNA. The PCR reaction mixture was initially denatured at 94°C for 10 min, followed by 35 cycles of 94°C for 1 min, 48 to 61°C (depending on annealing temperature specific to each primer pair) for 1 min, 72°C for 2 min, with a final extension step of 72°C for 10 min and 4°C indefinitely. The PCR thermal cycling was performed using the GeneAmp PCR system 9700 (Applied Biosystems, Foster City, CA). About 5 µL of 3x loading buffer (0.02 g bromophenol blue, 0.02 g xylene cyanol, 1.6 mL of 0.5 mol/L ethylenediamine tetraacetic acid [EDTA], and 38.4 mL formamide) was added to the PCR products to make a final volume of 15 µL. Before gel loading, samples were denatured for 5 min at 95°C and chilled on ice. The PCR products were separated by performing electrophoresis on polyacrylamide gels (6% [w/v] 20:1 acrylamide/bisacrylamide, 8 mol/L urea in TBE buffer, pH 8.3) in 1x TBE buffer (90 mmol/L Tris-borate (pH 8.3), 2 mmol/L EDTA) using PowerPac 3000 (Bio-Rad Laboratories, Hercules, CA) at a constant power of 110 W for 90 min. Gels were Ag stained by following the protocol described by Bassam et al. (1991) and photographed using automatic processor compatible film (Promega Corp., Madison, WI).

Genetic Linkage Analysis
For genetic analysis of the Sr9a allele, the band scores of all F₂ individuals were classified as being parental types or heterozygous. Analysis of the segregation pattern of Sr9a in the F₂ population and F₃ families was based on a ² distribution analysis used to test if the observed segregation ratios of homozygous resistant, heterozygous, and homozygous susceptible phenotypes fit the Mendelian ratios of 3:1 (F₃) or 1:2:1 (F₂) that would be expected if the resistance phenotype was controlled by a single dominant gene. Genetic linkage analysis was performed using Mapmaker Version 3.0b with the linkage groups based on a logarithm of odds score of at least 3.0. A partial genetic linkage map of chromosome 2BL was constructed using genetic distance in centimorgans (cM) as described by the Kosambi mapping function (Lander et al., 1987).

Informativeness of Polymorphic Microsatellite Markers
Fifty-nine wheat cultivars and breeding lines of diverse genetic origin (Table 1) were used to determine the informativeness of the SSR markers by calculating their polymorphism information content (PIC) according to the formula described by Anderson et al. (1993).

	RESULTS

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Phenotype and Segregation Analysis of the F₂ Population
The Sr9a-containing NIL parent ISr9a-Ra showed a resistant infection type of 2, whereas the recurrent parent Chinese Spring showed a susceptible infection type of 3+ to 4 against the TPMK and MCCF races of the stem rust pathogen. Among the 116 F₂ plants, 37 were homozygous resistant, 46 were heterozygous, and 33 were homozygous susceptible on the basis of reactions to both TPMK and MCCF races of F_2:3 families after inoculation with MCCF (Table 2 ). The ratio of 37:46:33 was consistent with the expected Mendelian segregation ratio of 1:2:1 with ² = 5.24 (P = 0.073), indicating that the F₂ population segregated for a single dominant gene conferring resistance.

View larger version (66K): [in this window] [in a new window]   Figure 1. Polyacrylamide gel electrophoresis showing the segregation pattern of the four microsatellite markers (A) Xgwm47, (B) Xgwm120, (C) Xbarc101, and (D) Xwmc175 in a subset of the F2 progenies from a cross between Sr9a near-isogenic lines (‘Chinese Spring’ and ISr9a-Ra); M is a 10-base pair (bp) ladder, 1 is resistant parent ISr9a-Ra, 2 is susceptible parent Chinese Spring, R is resistant F2 progeny, S is susceptible F2 progeny, and H is heterozygous resistant F2 progeny. Arrowheads indicate the size of the band associated with the Sr9a gene in coupling linkage (A–C) and also in repulsive linkage (D). Recombination or crossing over between the marker allele and the resistance allele is indicated by X.

View larger version (13K): [in this window] [in a new window]   Figure 2. A genetic linkage map of the Sr9a locus and the linked simple sequence repeat markers on the long arm of chromosome 2BL. The linkage map was constructed using 116 F2 individuals derived from a cross between near-isogenic lines (‘Chinese Spring’ and ISr9a-Ra). Names of markers and the gene are shown on the right.

The amplified band (190 base pairs [bp]) of Xgwm47 was associated with the presence of Sr9a in the breeding lines and accessions that were known to carry Sr9a, including ISr9a-Ra, Sr9a/9*LMPG, Marquis9*/Red Egyptian, and Red Egyptian as the original source of Sr9a (Table 1). Out of five accessions of Red Egyptian, PI 45403 showed a susceptible infection type (4) to race MCCF, indicating that this accession did not carry Sr9a, and this concurred with the absence of the Sr9a-specific marker allele at the Xgwm47 locus (Table 1). The Xgwm47 fragment size varied in most accessions that were known to be non-Sr9a-carrying lines. The fragment size of Xgwm120, Xbarc101, and Xwmc 175 varied among accessions and breeding lines, and was not associated with the presence of Sr9a in breeding lines known to carry Sr9a (Table 1).

	DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Sears (1962) used a chromosome substitution approach to locate Sr9a on chromosome 2B, and Sr9a was later mapped on the long arm of chromosome 2B using a telocentric mapping approach (Sears 1966b). The stem rust resistance gene Sr9a was identified as part of several alleles that form an allelic series complex at the Sr9 locus (Knott, 1989). The Sr9 locus and two other stripe rust resistance genes, Yr7 and Yr5, have been cytologically mapped on chromosome 2B with the same recombination frequency of 15 cM from the centromere (Hart et al., 1993), indicating that these loci were linked. Markers have been identified for Yr5 (Chen et al., 2003; Yan et al., 2003). In our laboratory, studies are in progress to determine if these sequence tagged site markers can be useful for genetic analysis of the allelic complex at the Sr9 locus.

We determined the location of Sr9a based on the available genetic maps of microsatellite markers. The use of NILs (ISr9a-Ra and Chinese Spring) facilitated the identification of the closest molecular markers, since the two lines have the same genetic background but differ in the presence of the Sr9a allele. Given the moderate- to high-density coverage of DNA markers on chromosome 2BL (Röder et al., 1998; Somers et al., 2004; Song et al., 2005), a partial linkage map constructed in this study indicated the marker Xgwm47 as being closely linked to Sr9a. These codominant markers were easy to score on polyacrylamide gels, with the exception of Xgwm120, which appeared as a faint band and required replication to verify the genotype of the marker allele. There were no codominant markers mapped to the distal side of Sr9a, however, owing to a lack of polymorphism rather than a lack of marker coverage. The order of markers in the current study shows some homologies with the map reported by Somers et al. (2004). Out of the four markers, the order of three markers corresponds to that reported by Somers et al. (2004). According to Song et al. (2005), however, the map location of Xbarc101 was found to be distal to the other markers, which conflicts with the order of markers reported by Somers et al. (2004). In our study, however, we observed no recombination between Xbarc101 and Xgwm120, and the two markers are proximal to Xgwm47 and Xwmc175. Therefore, our results are more consistent with the order of Somers et al. (2004) than Song et al. (2005). According to Somers et al. (2004), Xwmc175 mapped distal to Xgwm47, the same orientation as in Fig. 2. Based on these observations, at this stage we concluded that Sr9a is located distal to or in the vicinity of Xgwm47 and Xwmc175 (Fig. 2). The Xwmc175 and Sr9a alleles were in complete repulsion linkage. Perhaps this marker also may be useful in selecting individuals that are only homozygous for Sr9a. It is often desired to differentiate heterozygous from susceptible individuals, however, indicating a preference for the codominant Xgwm47.

Because Sr9a shows a moderately resistant reaction to common stem rust races in North America, it may be difficult to detect with phenotypic screening of heterozygous individuals in one generation, which prompts testing further generations. We overcame this complication by inoculating the F_2:3 families with race MCCF to distinguish and verify the F₂ genotypes. In postulating resistance genes, specific races are required to detect all or specific resistance genes. This requires all individuals to be inoculated with different races—a process that becomes time consuming and laborious. If there are only a few races available to detect all combinations of resistance genes, however, masking effects due to other Sr genes cannot be avoided. The problem of detecting the Sr9a allele has restricted its use in breeding programs. On the other hand, the Sr9a allele does not confer resistance to some races, so there is a need to combine it with other stem rust resistance genes, a process that can be achieved with the use of molecular markers. This will, therefore, avoid the use of a large number of races required to postulate the presence of individual Sr genes, in this case Sr9a, when it is combined with other Sr genes. With MAS, it is possible to develop cultivars with a more broad-based resistance against a wide range of races (Eagles et al., 2001).

The marker alleles of Xgwm120, Xbarc101, and Xwmc175 varied among accessions and breeding lines, and were not associated with the presence of Sr9a in resistant breeding lines known to carry Sr9a. This indicates that the linkage of these marker loci with Sr9a had been broken because the breeding lines in this study have undergone several generations of recombination and selfing during inbred line development. The Xgwm47 marker, however, displayed a marker allele (190 bp) that was specific to Red Egyptian and was validated in all NILs tested. Even though there was recombination between the markers and the Sr9a gene, the marker Xgwm47 should be valuable for MAS because of its diagnostic 190-bp allele and relatively high PIC value. Markers Xgwm120, Xbarc101, and Xwmc175 may also be good candidates for MAS if the parents are polymorphic for the marker alleles and one parent is known to contain Sr9a.

In the analysis of these accessions, we also tried to postulate the presence of Sr9a on the basis of gene-for-gene specificity. There are obvious limitations to this approach of postulating stem rust resistance genes in wheat, and in this study some of the accessions showed very low infection type against all three races (QFCS, TPMK, and MCCF). Hence, we cannot rule out the possibility that some of these accessions may possess the Sr9a gene because it could have been masked by other Sr genes. Based on these results, further genetic analysis is required to determine if some of the accessions are carriers or noncarriers of Sr9a. These include ‘Centurk’, ‘Lerma Rojo 64’, ‘NC-Neuse’, and ‘Excel’. The Centurk and Lerma Rojo 64 cultivars were reported as carriers of Sr9a together with other genes, including Sr2, Sr5, Sr6, Sr7b, Sr8a, and Sr17 (Roelfs, 1988b; McIntosh et al., 1995); however, these cultivars show a non-Sr9a-specific marker allele at the Xgwm47 locus. Our results showed that ‘Vista’ has a Sr9a-specific marker allele at the Xgwm47 locus, and this allele might have been inherited from Centurk; however, Centurk did not display the Sr9a-linked marker allele (Table 1). One possible explanation is that the Centurk cultivar may be heterogeneous for Sr9a.

In summary, although Sr9a does not provide a high level of resistance against a wide range of rust races on its own, it can still be a valuable gene when pyramided with other stem rust resistance genes. Moreover, the Sr9a gene provides resistance to TPMK, which once was the most common race of stem rust in the USA for many years. The SSR marker Xgwm47 or other markers identified in this study may be used to pyramid Sr9a with other Sr genes from different resistance sources into a single line during cultivar development. It may also be possible that the linkage between the Sr9a gene and other multiple alleles at the Sr9 locus can permit an efficient transfer of any one of these alleles based on Xgwm47.

	ACKNOWLEDGMENTS

 
We would like to thank Lucille Wanschura for her assistance in preparing the stem rust inoculum and all members of the wheat breeding project who helped in various stages of the project. This research was funded in part by the Minnesota Annual Conference of the United Methodist Church and the Agricultural Research Council of South Africa.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.

Research supported in part by the Minnesota Annual Conference of the United Methodist Church through the Project AgGrad fellowship awarded to T.J. Tsilo

Received for publication February 15, 2007.

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